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Published in final edited form as: Curr Opin Neurobiol. 2022 Apr 27;74:102548. doi: 10.1016/j.conb.2022.102548

Tactile sensation in birds: Physiological insights from avian mechanoreceptors

Luke H Ziolkowski 1, Elena O Gracheva 1,2,3,*, Sviatoslav N Bagriantsev 1,*
PMCID: PMC9167745  NIHMSID: NIHMS1796044  PMID: 35489134

Abstract

The sense of touch is ubiquitous in vertebrates, and relies upon the detection of mechanical forces in the skin by the tactile end-organs of low-threshold mechanoreceptors. Significant progress has been made in understanding the mechanism of tactile end-organ function using mammalian models, but the detailed mechanics of touch sensation in Meissner and Pacinian corpuscles, the principal detectors of transient touch and vibration, remain obscure. The avian homologues of these corpuscles present an opportunity for functional study of mechanosensation in these structures, due to their relative accessibility and high abundance in the bill skin of tactile foraging waterfowl. Here, we review the current knowledge of mechanosensory end-organs in birds, and highlight the utility of the avian model to understand general principles of touch detection in glabrous skin of vertebrates.

Introduction

The sensation of non-painful touch in vertebrates is mediated by low threshold mechanoreceptors (LTMRs), pseudounipolar somatosensory neurons originating from the dorsal root ganglia or the trigeminal ganglia. Somatosensory afferents projecting from LTMRs detect mechanical stimuli in the skin and transmit tactile information through the corresponding somatosensory pathways in the central nervous system. In glabrous skin, such as that covering the human palm, LTMRs form four types of terminal end-organs: the Pacinian corpuscle, the Meissner corpuscle, the Ruffini corpuscle, and the Merkel cell-neurite complex. Comprehensive reviews on these mechanoreceptors and mechanotransduction in mammals can be found elsewhere [1–4]. Here we will focus on the current knowledge of these mechanoreceptors in birds, with an emphasis on the avian homologues of Pacinian and Meissner corpuscles, the principal detectors of transient touch and vibration. Furthermore, we will highlight the potential of avian model organisms to contribute to our understanding of each tactile end-organ and vertebrate mechanosensation as a whole.

While much of what is known about the structure and function of LTMRs has been acquired from research on mammals, birds provide a particularly useful and underutilized model to study tactile sensation. Many mechanosensory mechanisms and structures are conserved across vertebrates. Similar to mammalian mechanoreceptors, avian LTMRs can be classified as slowly-adapting (SA) or rapidly-adapting (RA) receptors, depending on their firing pattern in response to mechanical stimulation. The most prominent and well-studied end-organs in birds are Grandry and Herbst corpuscles, which are innervated by RA-LTMRs, and are structurally and functionally analogous to, respectively, Meissner and Pacinian corpuscles found in mammals [5–7]. Merkel cell-neurite complexes and Ruffini corpuscles, which are innervated by SA-LTMRs, are also found in birds, although their structure, location, and density may vary among species [8].

Mechanosensory end-organs are complex structures composed of the LTMR afferent and non-neuronal cells, such as Merkel cells or various types of lamellar cells. Traditionally, the afferent has been thought of as the sole mechanoreceptive entity within end-organs, whereas the non-neuronal components have been thought to play supportive and regulatory roles [9]. However, studies in mice have revealed that Merkel cells detect touch and modulate the function of the afferent [10–12], challenging this traditional view. Meanwhile, the role of the non-neuronal components in Meissner and Pacinian corpuscles is less clear, because these structures are poorly accessible to direct functional studies in mouse skin. In precocial birds, such as ducks, the development of the somatosensory system largely completes before hatching [13,14], which permits electrophysiological analysis of the non-neuronal components of mechanosensory end-organs using the skin of late-stage embryos [7]. Because of this advantage, birds provide a unique opportunity to study LTMRs and understand the basic principles of touch detection in vertebrates.

Mechanosensation in avian species

The sense of touch is indispensable to the survival of many forms of life, and birds are no exception. Just as some fish, reptiles, and mammals have evolved specialized mechanosensory organs [15–17], some birds have done so as well. In many avian species, the bill or beak has emerged as this tactile organ, and a fine sense of touch may extend to the tongue [18–21] and oropharynx [22]. In many waterfowl of the Anatidae family, which includes ducks (Figure 1a), swans, and geese, Grandry and Herbst corpuscles are present at an exceptionally high density in the skin covering the bill (Figure 1b–c), tongue and oral cavity, and are thought to underlie sophisticated tactile-based foraging [17,23–25]. In the Mallard duck (Anas platyrhynchos), bill-localized mechanosensation is required for effective feeding in a dark environment, where the sense of touch dominates foraging behavior [26]. Similarly, the New Zealand kiwi (Apteryx mantelli) relies upon tactile foraging in lieu of visually-guided foraging, utilizing the mechanoreceptors and corpuscles located in its bill [27,28]. Behavioral and anatomical evidence for a specialized mechanosensory bill/beak also exists in other birds, including emus, ostriches [22], finches [29–31], ibises [32], parrots [33], and various shorebirds [34], but mechanosensation may be enhanced in some species compared to others. Indeed, tactile specialist birds have a significantly higher proportion of mechanoreceptors in their trigeminal ganglia compared to visual foragers [35], and display a larger volume of the trigeminal nucleus, the brainstem region that perform the initial processing of sensory information from trigeminal LTMRs [36,37]. Consequently, in many of these specialist species, especially tactile-foraging ducks, the mechanosensory function of the bill can be considered equivalent to that of the human hand. As most of our understanding of the physiology of peripheral mechanotransduction in the skin of birds comes from tactile specialist waterfowl, we will focus on them when discussing the function of cutaneous LTMRs.

Figure 1. The structure and function of Grandry and Herbst corpuscles within the mechanosensory bill of waterfowl.

Figure 1.

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(a) The neuroanatomy underlying tactile sensation in the bill. LTMRs from the trigeminal ganglia (TG) project to the skin of the bill. (b) Trigeminal LTMRs form terminal end-organs in the bill dermis, most of which are Grandry and Herbst corpuscles. (c) Image of the bill dermis under a brightfield microscope. Grandry (yellow arrows) and Herbst (red arrows) corpuscles are present at a cumulative density of up to 200 corpuscles per square millimeter of skin, and can be easily distinguished by size and morphology. (d) Higher magnification image and diagram of a Grandry corpuscle. The Grandry corpuscle is composed of 2–12 lamellar cells which are layered above and below the terminals of the RA-LTMR. The structure is encapsulated by satellite cells. Below the diagram, example stimuli (black) and LTMR afferent responses (blue) are shown. The LTMR of the Grandry corpuscle detects changes in transient force, low frequency vibration, and velocity; the impulses/second of the LTMR response increase with increasing velocity of the mechanical stimulus. (e) Higher magnification image and diagram of a Herbst corpuscle. The Herbst corpuscle is composed of an outer capsule formed by outer core lamellar cells, which encloses an inner core comprised of inner core lamellar cells. The outer core and inner core lamellar cells form concentric lamellae surrounding the mechanoreceptor afferent. Below the diagram, example stimuli (black) and LTMR afferent responses (blue) are shown. The LTMR of Herbst corpuscles detects transient force and high frequency vibration.

Importantly, the major molecular mechanism of mechanotransduction in LTMRs appears to be conserved between birds and mammals. In Pekin ducks, the domesticated descendants of the Mallard, the mechanosensitive ion channel Piezo2 [38] mediates a portion of the excitatory mechanically activated (MA) current in somatosensory neurons [14], and is likely responsible for mechanotransduction in a subset of avian LTMRs, as it is in mice [39]. There is a significant increase in the duration of Piezo2-mediated MA current in duck mechanoreceptors compared to mice [14], the consequences of which are not yet clear, but it is possible that the longer-lasting MA current increases the chance of action potential firing in response to a light mechanical stimulus. When assayed in heterologous cells, most functional properties of duck Piezo2 appear to be highly conserved with mammalian orthologues, including fast inactivation [14] and cold-induced potentiation [40] of MA current. Additionally, Piezo2 is expressed in a large proportion of duck TG neurons, which display larger MA currents compared to other birds and mice [35,41]. This likely reflects the incredibly high density of trigeminal RA-LTMRs and associated sensory corpuscles in the bill (Figure 1b,c). Because of these conserved mechanisms and physiological advantages, investigation into the LTMRs and end-organs of avian tactile specialists may yield valuable insight into the function of these structures across vertebrates.

Grandry (Meissner-like) corpuscle

Grandry corpuscles are ovoid end-organs innervated by RA-LTMRs that detect velocity and low frequency vibration (Figure 1d) [5,6]. These structures are found in the bill of waterfowl at a density up to 65 corpuscles per square millimeter [23]. Grandry corpuscles contain as few as two lamellar cells that surround the nerve ending [7], although this number can be as high as 12 in some species [6]. The lamellar cells are derived from Schwann cells and form a stacked column in which nerve endings are sandwiched between pairs of cells, altogether encapsulated by satellite cells [13,23,42]. Similar formations called “Merkel corpuscles” have been previously characterized in nonaquatic birds, but these often bear a striking morphological resemblance to Grandry and Meissner corpuscles [31] and they are likely variations of the same structure [43] which are distinct from Merkel cell-neurite complexes. As stated previously, Grandry corpuscles are analogous to the Meissner corpuscle, the type II RA-LTMR of mammals.

Similar to the Grandry corpuscle, Meissner corpuscles detect velocity and low frequency vibration [44,45]. These structures are found in the glabrous skin of the human and primate hands [2,46] and mouse paws [47,48]. The nerve ending of the Meissner corpuscle is also surrounded by several lamellar cells of Schwann cell origin [9,49,50]. Interestingly, Meissner corpuscles are often innervated by more than one type of neuron [44,51,52], which can have different responses to the same mechanical stimulus [44]. It remains to be seen whether this multifaceted innervation and divergent physiology is present in the Grandry corpuscle of birds. Additionally, mammalian Meissner corpuscles are innervated by RA-LTMR afferents that express the mechanically gated ion channel Piezo2 [39,53]. Even though Piezo2 is expressed in ~70% of trigeminal neurons of the tactile specialist Pekin duck [14], whether Grandry corpuscles are innervated by Piezo2-expressing afferents remains to be tested.

Lamellar cells in Grandry and Meissner corpuscles are thought to be important for their function, though their exact role is currently obscure. The afferent is typically considered the sole entity within corpuscles that detects touch, whereas the role of lamellar cells is thought be auxiliary and supportive. A recent study showed USH2A, a putative tether protein which is implicated in human hearing and inner ear function [54,55], is not only expressed in lamellar cells of Meissner corpuscles, but necessary for vibration detection and proper function of the mechanoreceptor in mice [45]. This suggests that the lamellar cell may act as an anchor that supports mechanotransduction in the nerve ending by a yet unknown mechanism. Alternatively, or in addition, lamellar cells could actively participate in touch detection, and shape the response of the afferent, similar to the paradigm discovered in Merkel cell-neurite complexes, whereby both the Merkel cells and the afferent detect touch [10–12]. This idea is supported by a recent electrophysiological investigation of the lamellar cells of Grandry corpuscles in duck bill skin [7]. It was shown that mechanical stimulation triggers depolarization in lamellar cells via opening of mechanically gated ion channels of a yet unidentified type. This leads to generation of action potentials in lamellar cells via R-type voltage-gated calcium channels. Although lamellar cells detect touch, it remains unclear how, if at all, they communicate the tactile information with the afferent. Numerous large dense-core vesicles in these cells can be detected in the cytosol of lamellar cells using electron microscopy [7,56], raising the possibility that the lamellar cells help transduce mechanical forces and induce/modulate the afferent response via a chemical secretory mechanism, similar to the Merkel cell-neurite complex characterized in mice [57,58].

Herbst (Pacinian-like) corpuscle

In many birds, including tactile specialist waterfowl, Herbst corpuscles are the most common end-organ encountered in the skin. Herbst corpuscles are present throughout the class Aves [6,18,22,23,29,30,32,34,59–61], but as mentioned previously, have an incredibly high density in the bills of ducks [23] and geese [6], up to 140 corpuscles per square millimeter. Herbst (and Pacinian) corpuscles are ellipsoid structures composed of multiple layers of lamellar cells that surround the terminal of RA-LTMRs (distinct from Grandry-innervated RA-LTMRs), which detect high frequency vibration (Figure 1e). An outer capsule is formed by several concentric lamellae made up of flattened cells referred to as “outer core lamellar cells.” This capsule surrounds the inner core, a bilateral row of Schwann cell-derived “inner core lamellar cells” which extend complex, interdigitating lamellae around the nerve terminal at the center of the corpuscle [56].

Similarly, the mammalian Pacinian corpuscle has an encapsulated, lamellar structure and is present at varying densities in glabrous skin and other tissues, depending on the species. These corpuscles are found in the human hand [2,62], the mesentery of cats [63], and the foot/paw of many other mammals, including dogs [64], raccoons [65], and elephants [66]. However, Pacinian corpuscles are restricted to the joints [67] and periosteum [68] of rodents and are less experimentally accessible compared to the Herbst corpuscles in the bill of waterfowl [6,23]. Physiological data and computational models show that despite differences in size and number of outer lamellae, both the mammalian Pacinian corpuscle and avian Herbst corpuscle are rapidly adapting and tuned to high frequency vibration [5,69–71]. Thus, though there is some structural variation between the end-organs, their basic microanatomical features and functional roles are very similar.

The lamellar cells of the Herbst and Pacinian corpuscles are thought to be an integral passive component responsible for shaping the mechanical forces experienced by the nerve at the center of the structure. Removing the outer layers of these cells from the end-organ prolongs the generator potential produced by mechanically gated channels in the neuron of cat Pacinian corpuscles [72]. At the same time, lamellar cells possibly play a more active role in lamellated corpuscle signal transduction. Potential evidence for such a role exists in the Herbst corpuscle; lamellar cells of the outer layers of this corpuscle respond to touch in the form of MA current [7]. However, these lamellar cells lack voltage-gated ion channels and are located far from the neuron, so the functional consequences of their mechanosensitivity is unclear. It is possible that the MA current in these cells is important for mechanotransduction of the corpuscle as a whole, but this remains to be shown. Further work in this system is warranted to investigate the functional role of these lamellar cells in Herbst/Pacinian corpuscles and identify the molecule(s) responsible for their MA current.

The lamellar cells of the inner core of the Herbst corpuscle are also potentially critical: they form close junctions with the afferent via a complex network of thin lamellae. Additionally, these inner core cells express various calcium binding proteins [73,74] and the ion channels Trpv4 and Asic2 [75], which could have some physiological purpose within the corpuscle. Immunohistochemical and functional studies suggest a possible mechanochemical synaptic-like communication between inner core cells and the afferent in Pacinian corpuscles [76,77], but direct evidence for active touch detection in inner core cells is missing. Importantly, the structure of the inner core is mostly complete at embryonic days 24–28 in ducks [78], the time at which Herbst corpuscles are functional. At this stage, electron micrographs show vesicles and high density junctions located near membranes of the inner core, though it is unclear if these structures are located in the nerve terminal or lamellae of inner core cells [79]. While the outer lamellar cells could previously be removed from the cat Pacinian corpuscle, it was impossible to remove all of the inner core structure [80], and thus it was impossible to test the function of the inner core cells. The Herbst corpuscle may act as a more flexible experimental medium for investigating the inner core given the corpuscle’s accessibility and density in the duck bill. It would be worthwhile to know whether inner core cells can detect touch, and whether they play a role in shaping afferent responses, given their intimate association with the nerve terminal. However, electrophysiological properties of inner core lamellar cells have not been reported in any species.

Ruffini corpuscle and the Merkel cell-neurite complex

Ruffini corpuscles are traditionally considered to be innervated by type II SA-LTMRs, though this association is questionable due to discrepancies between physiological and anatomical data [81]. These structures are rare and difficult to identify in many species, including humans [81,82], and thus pose a challenge to investigate in any organism. Merkel cell-neurite complexes, on the other hand, are well characterized from studies in mammals, and are known to be innervated by type I SA-LTMRs. Recent work has revealed that in both hair follicles and touch domes of mice, Merkel cells detect mechanical stimuli and help shape the responses of corresponding afferents to touch [10–12]. A chemical synapse between the Merkel cell and the afferent mediates this interaction. In mice, this synapse has been reported to be either serotonergic or adrenergic [57,58]. It is unclear if avian Merkel cells perform a similar function, due to the absence of functional knowledge of these receptors in birds.

While physiological investigation of Ruffini corpuscles and Merkel-cell neurite complexes in birds is lacking, some anatomical and structural studies have been performed. Histological and ultrastructural evidence of Ruffini corpuscles and Merkel cells has been found in bill/beak skin and oral mucosa of the Muscovy duck (Cairina moschata) and Japanese quail (Corturnix coturnix japonica) [8,83], though both end-organs were rarer in the former. Confusion exists around the existence and identity of the avian Merkel cell-neurite complex due to the presence of previously mentioned “Merkel corpuscles,” which more closely resemble mammalian Meissner corpuscles and Grandry corpuscles of waterfowl [31]. Merkel cells can be found independent of these structures in the duck [84]; these cells may be more closely related to the Merkel cell-neurite complex seen in mammals. In the shoulder joint of the domestic pigeon (Columba livia domestica), Ruffini corpuscles were also identified [61], but it is unclear how common they are in other anatomical locations such as the beak. Within the avian Ruffini corpuscle, the nerve terminal forms a complex branching structure surrounded by specialized terminal Schwann cells and fibrous elements [82,83], components also seen in the Pacinian, Meissner, Herbst, and Grandry corpuscles. The function of these Schwann-like cells of Ruffini corpuscles and Merkel cells in birds is still unknown. Further investigation of the Ruffini corpuscle and the Merkel cell-neurite complex across different species may provide insight into evolutionarily conserved mechanisms of mechanotransduction and physiological properties of these mechanoreceptors.

Concluding remarks

Many questions remain about the precise physiological workings of vertebrate LTMRs. Of particular interest is the role of lamellar cells in the Herbst (Pacinian) and Grandry (Meissner) corpuscles. Thorough functional studies will be required to dissect the cellular and molecular mechanisms by which the neuronal and non-neuronal components of these end-organs interact with each other and transduce mechanical stimuli. Because of the high density and experimental accessibility of Grandry and Herbst corpuscles in tactile-foraging birds, these organisms remain powerful experimental models with which to study rapidly adapting mechanoreceptors. Avian species will be further useful for exploring conserved mechanisms of mechanosensation found throughout various vertebrate organisms and touch receptors.

Highlights.

  • The neurophysiology of touch sensation is conserved across birds and mammals

  • Bird mechanoreceptors innervate Grandry (Meissner) and Herbst (Pacinian) corpuscles

  • Grandry and Herbst corpuscles densely populate the bill skin of tactile foragers

  • Grandry and Herbst corpuscles detect transient touch, velocity, and vibration

  • Lamellar cells are critical to sensory corpuscle structure and function

Acknowledgements

This work was supported by NSF grant 1754286 to E.O.G., NSF grants 1923127, and NIH grant 1R01NS097547 to S.N.B. We thank Dr. Yury Nikolaev for contributing microscopy images.

Footnotes

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Conflict of interest statement

None declared.

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